Colorectal Cancer Stage at Diagnosis Before vs During the COVID-19 Pandemic in Italy

Author:

Rottoli Matteo12,Gori Alice12,Pellino Gianluca34,Flacco Maria Elena5,Martellucci Cecilia5,Spinelli Antonino67,Poggioli Gilberto12,Romano Angela8,Belvedere Angela8,Lanci Lanci Antonio8,Parlanti Daniele8,Vago Gabriele8,Pezzuto Paola8,Canavese Anna8,Dajti Gerti8,Cardelli Stefano8,Catalioto Caterina8,Russo Iris S8,Violante Tommaso8,Morezzi Daniele8,Maurino Ludovica8,Filippone Eleonora8,Cuicchi Dajana8,Bernante Paolo8,Jovine Elio8,Lombardi Raffaele8,Masetti Michele8,Cipressi Chiara8,Offi Maria F8,Larotonda Cristina8,Puglisi Silvana B8,Barbosa Augusto8,Vaiana Roberto8,Bianchi Paolo M8,Tonti Carlo8,Codignola Claudio8,Zorcolo Luigi8,Restivo Angelo8,Deidda Simona8,Marchetti Marcello E8,Ippolito Luca8,Spolverato Gaya8,Pucciarelli Salvatore8,Marchegiani Francesco8,Ghio Giacomo8,Zagolin Gaya8,Glavas Dajana8,Tomassi Monica8,Rosati Riccardo8,Elmore Ugo8,Gozzini Lorenzo8,Calef Riccardo8,Puccetti Francesco8,Cossu Andrea8,Vignali Andrea8,Morino Mario8,Allaix Marco E8,Cannata Gaspare8,Lombardi Erica8,Ammirati Carlo A8,Piceni Chiara8,Buccianti Piero8,Balestri Riccardo8,Puccini Marco8,Pezzati Daniele8,d'Ischia Roberto8,Asta Vito F8,Sargenti Benedetta8,Taddei Giacomo8,Bonari Federica8,Boni Giulia8,Ferrero Alessandro8,Mineccia Michela8,Gonella Federica8,Palisi Marco8,Danese Francesco8,Cherubini Valeria8,Perotti Serena8,Carvello Michele8,Carbone Fabio8,Luberto Antonio8,Calafiore Eleonora8,De Lucia Francesca8,Sacchi Matteo8,Sasia Diego8,Giuffrida Maria C8,Ballauri Edoardo8,Cardile Mathieu8,Armentano Serena8,Beltrami Elsa8,Preve Gabriele8,Vercellone Barbara8,Mozzon Marta8,Folliero Cristina8,Lirusso Chiara8,Vecchiato Massimo8,Ziccarelli Antonio8,Gattesco Davide8,Moretti Luisa8,Crestale Sara8,Banchini Filippo8,Capelli Patrizio8,Romboli Andrea8,Palmieri Gerardo8,Conti Luigi8,Rizzi Nicholas8,Bonfili Deborah8,de Manzini Nicolò8,Germani Paola8,Osenda Edoardo8,Cortinovis Sara8,Giunta Carlotta8,Fracon Stefano8,Abdallah Hussein8,Bogoni Selene8,Portolani Nazario8,Nascimbeni Riccardo8,Molfino Sarah8,Tiberio Guido A M8,Garosio Ilenia8,Lamperti Giulia8,Rigosa Diego8,Ercolani Giorgio8,Solaini Leonardo8,Cavaliere Davide8,Avanzolini Andrea8,D'Acapito Fabrizio8,Chiarella Leonardo L8,Di Pietrantonio Daniela8,Annunziata Domenico8,Piccolo Roberta8,Sorrentino Mario8,Pansini Mauro8,Cojutti Alessandro8,Graziano Michele8,Callegari Francesco8,Balzarotti Laura8,Dameno Vitale R8,Cattaneo Antonio8,Santolamazza Giuliano8,Altieri Caterina8,Magarini Riccardo8,Pietrabissa Andrea8,Dominioni Tommaso8,Pugliese Luigi8,Peri Andrea8,Botti Marta8,Salvetti Francesco8,Cassinotti Elisa8,Baldari Ludovica8,Boni Luigi8,Messina Valentina8,D'Abrosca Vera8,Cianci Pasquale8,Tumolo Rocco8,Gattulli Domenico8,Restini Enrico8,Minafra Marina8,Sederino Maria G8,Bottalico Bernardino8,Pilati Pierluigi8,Franzato Boris8,Mattara Genny8,De Simoni Ottavia8,Barina Andrea8,Tonello Marco8,Muratore Andrea8,Calabrò Marcello8,Federico Pipitone Nicoletta S8,Cuzzola Bruno8,Herranz van Nood Elena8,Passuello Nicola8,Frasson Alvise8,Mammano Enzo8,Faccio Luca8,Vittadello Fabrizio8,Bressan Alice8,Sarzo Giacomo8,Tamini Nicolò8,Oldani Massimo8,Cigagna Luca8,Carissimi Francesca8,De Carlo Giulia8,Baccalini Edoardo8,Nespoli Luca8,Giordano Alessio8,Cantafio Stefano8,Grifoni Lucrezia8,Matani Davide8,Livi Serena8,Delogu Daniele8,Scognamillo Fabrizio8,Marrosu Antonio8,Guerrini Luca8,Ugolini Giampaolo8,Ghignone Federico8,Frascaroli Giacomo8,Albertini Nicola8,Zattoni Davide8,Taffurelli Giovanni8,Montroni Isacco8,Colombo Francesco8,Danelli Piergiorgio8,Bondurri Andrea8,Maffioli Anna8,Bonomi Alessandro8,Pezzoli Isabella8,Cammarata Francesco8,Goletti Orlando8,Molteni Mattia8,Assisi Alberto8,Quartierini Giorgio8,Da Lio Corrado8,Verdi Daunia8,Mondi Isabella8,Peluso Claudia8,Macchi Lorenzo8,Tanzanu Marta8,Zanzi Federico8,Pellegrini Sara8,Andreuccetti Jacopo8,D'Alessio Rossella8,Pignata Giusto8,De Capua Michele8,Canfora Ilaria8,Ottaviani Luca8,Lepiane Pasquale8,Balla Andrea8,De Carlo Antonio8,Saraceno Federica8,Scaramuzzo Rosa8,Guida Anna8,Aguzzi Daniele8,Bellora Paolo8,Gentilli Sergio8,Monni Manuela8,Nikaj Herald8,Cillara Nicola8,Cannavera Alessandro8,Deserra Antonello8,Margiani Carla8,Cabula Roberta8,Dettori Manuela8,Gramignano Giulia8,Lezoche Giovanni8,Ortenzi Monica8,Orlandoni Elena S8,Curzi Federica8,Vitali Francesca8,Capomagi Perla8,Palmieri Miriam8,Giuffrida Mario8,Del Rio Paolo8,Bonati Elena8,Loderer Tommaso8,Cozzani Federico8,Rossini Matteo8,Agnesi Stefano8,Capolupo Gabriella T8,Caricato Marco8,Carannante Filippo8,Mascianà Gianluca8,Marrelli Martina8,Miacci Valentina8,Lauricella Sara8,Tonini Valeria8,Cervellera Maurizio8,Pisconti Salvatore8,Lozito Concetta8,Shahu Juliana8,Mongelli Claudia8,Morelli Giulia8,Sartarelli Lodovico8,Sica Giuseppe S8,Siragusa Leandro8,Bagaglini Giulia8,Sensi Bruno8,Guida Andrea M8,Franceschilli Marzia8,Vinci Danilo8,Taddei Antonio8,Risaliti Matteo8,Bartolini Ilenia8,Ringressi Maria N8,Tirloni Luca8,Laface Letizia8,Abate Emmanuele8,Casati Massimiliano8,Gobbi Pietro8,Opocher Enrico8,Mariani Nicolò M8,Pisani Ceretti Andrea8,Giovenzana Marco8,Giuliani Beatrice8,Sironi Martina8,Grossi Ugo8,Zanus Giacomo8,Aniello Santoro Giulio8,Brizzolari Marco8,De Leo Eugenio8,Novello Simone8,Aquilino Krizia8,Milardi Francesco8,Olmi Stefano8,Uccelli Matteo8,Bonaldi Marta8,Cesana Giovanni C8,Bindi Marco8,Galleano Raffaele8,Langone Antonio8,Botto Massimiliano8,Franceschi Angelo8,Gambino Elena8,Ronconi Maurizio8,Casiraghi Silvia8,Casole Giovanni8,Ciulla Salvatore L8,Terrosu Giovanni8,Calandra Sergio8,Scarpa Edoardo8,Cherchi Vittorio8,Calini Giacomo8,Martinuzzo Lisa8,Clocchiatti Lucrezia8,Muschitiello Davide8,Romanzi Andrea8,Vignati Barbara8,Vannelli Alberto8,Scolaro Roberta8,Milanesi Maria8,Rossi Fabrizio8,Canonico Giuseppe8,Anastasi Alessandro8,Nelli Tommaso8,Barlettai Marco8,Fratarcangeli Riccardo8,Di Martino Carmela8,Damigella Andrea8,Adinolfi Elvira8,Birindelli Arianna8,Taglietti Lucio8,Dester Sara E8,Fleres Francesco8,Cucinotta Eugenio8,Viscosi Francesca8,Biondo Santino Antonio8,Badessi Giorgio8,Catarsini Nivia8,Mazzeo Carmelo8,Rega Daniela8,Delrio Paolo8,Cervone Carmela8,Aversano Alessia8,De Franciscis Silvia8,Di Marzo Massimiliano8,Marra Bruno8,Pace Ugo8,Amato Antonio8,Batistotti Paola8,Mina Elisa8,Serventi Alberto8,Lapolla Pierfrancesco8,Mingoli Andrea8,Sapienza Paolo8,Brachini Gioia8,Cirillo Bruno8,Fiori Enrico8,Crocetti Daniele8,Clementi Ilaria8,Martines Gennaro8,Picciariello Arcangelo8,Tomasicchio Giovanni8,Dibra Rigers8,Trigiante Giuseppe8,Rinaldi Marcella8,Lantone Giuliano8,Porcu Alberto8,Perra Teresa8,Scanu Antonio M8,Feo Claudio F8,Fancellu Alessandro8,Cossu Maria L8,Ginesu Giorgio C8,Patriti Alberto8,Coletta Diego8,Petrelli Filippo8,Greco Paola A8,Spadoni Claudia8,Cassiani Giovanna8,Bianchini Federica8,Arganini Marco8,Bianchini Matteo8,Perotti Bruno8,Palmeri Matteo8,Scabini Stefano8,Deiana Selene8,Carganico Giacomo8,Pertile Davide8,Soriero Domenico8,Fioravanti Emanuela8,Sperotto Beatrice8,Nardo Bruno8,Paglione Daniele8,Crocco Veronica8,Doni Marco8,Osso Mariasara8,Perri Roberto8,Sampietro Gianluca M8,Corbellini Carlo8,Lorusso Leonardo8,Manzo Carlo A8,Cigognini Maria8,Baldi Caterina8,Palomba Giuseppe8,Aprea Giovanni8,Capuano Marianna8,Basile Raffaele8,Tutino Roberta8,Massani Marco8,Marinelli Laura8,Canitano Nicola8,Pilia Tiziana8,Podda Mauro8,Pisanu Adolfo8,Murzi Valentina8,Incani Silvia8,Frongia Federica8,Esposito Giuseppe8,Luglio Gaetano8,Tropeano Francesca P8,Pagano Gianluca8,Spina Eduardo8,De Simone Giuseppe8,Cricrì Michele8,Catena Fausto8,Vallicelli Carlo8,Zanini Nicola8,Ronconi Diana8,Favi Francesco8,Mazzucchelli Carlo8,Convertini Girolamo8,Vincenti Leonardo8,Andriola Valeria8,Bizzoca Cinzia8,Feo Carlo V8,Fabbri Nicolò8,Fazzin Marta8,Pesce Antonio8,Gennari Silvia8,Torchiaro Marco8,Severi Silvia8,Frontali Alice8,Bracchetti Greta8,Granieri Stefano8,Cotsoglou Christian8,Carlini Massimo8,Lisi Giorgio8,Spoletini Domenico8,Mastrangeli Maria R8,Campanelli Michela8,Manigrasso Michele8,Milone Marco8,De Palma Giovanni D8,Vertaldi Sara8,Chini Alessia8,Maione Francesco8,Marello Alessandra8,Selvaggi Francesco8,Sciaudone Guido8,Selvaggi Lucio8,Menegon Tasselli Francesco8,Fuschillo Giacomo8,Oddis Lidia8,Grande Simona8,Grande Michele8,Ascanelli Simona8,Chimisso Laura8,Aisoni Filippo8,Rossin Eleonora8,Pepe Francesco8,Marchetti Francesco8,Picardi Biagio8,Rossi Stefano8,Rossi Del Monte Simone8,Picarelli Matteo8,Muttillo Irnerio A8,Ratto Carlo8,Marra Angelo A8,Parello Angelo8,Litta Francesco8,Campennì Paola8,De Simone Veronica8,Pata Francesco8,Riboni Cristiana8,Rausa Emanuele8,Celentano Valerio8,

Affiliation:

1. Surgery of the Alimentary Tract, IRCCS Azienda Ospedaliero–Universitaria di Bologna, Bologna, Italy

2. Department of Medical and Surgical Sciences, Alma Mater Studiorum University of Bologna, Bologna, Italy

3. Department of Advanced Medical and Surgical Sciences, Università degli Studi della Campania Luigi Vanvitelli, Naples, Italy

4. Colorectal Surgery, University Hospital Vall d’Hebron, Barcelona, Spain

5. Department of Environmental and Preventive Sciences, University of Ferrara, Ferrara, Italy

6. Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, Milan, Italy

7. Colorectal Surgery, IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy

8. for the COVID–Colorectal Cancer (CRC) Study Group

Abstract

ImportanceDelays in screening programs and the reluctance of patients to seek medical attention because of the outbreak of SARS-CoV-2 could be associated with the risk of more advanced colorectal cancers at diagnosis.ObjectiveTo evaluate whether the SARS-CoV-2 pandemic was associated with more advanced oncologic stage and change in clinical presentation for patients with colorectal cancer.Design, Setting, and ParticipantsThis retrospective, multicenter cohort study included all 17 938 adult patients who underwent surgery for colorectal cancer from March 1, 2020, to December 31, 2021 (pandemic period), and from January 1, 2018, to February 29, 2020 (prepandemic period), in 81 participating centers in Italy, including tertiary centers and community hospitals. Follow-up was 30 days from surgery.ExposuresAny type of surgical procedure for colorectal cancer, including explorative surgery, palliative procedures, and atypical or segmental resections.Main Outcomes and MeasuresThe primary outcome was advanced stage of colorectal cancer at diagnosis. Secondary outcomes were distant metastasis, T4 stage, aggressive biology (defined as cancer with at least 1 of the following characteristics: signet ring cells, mucinous tumor, budding, lymphovascular invasion, perineural invasion, and lymphangitis), stenotic lesion, emergency surgery, and palliative surgery. The independent association between the pandemic period and the outcomes was assessed using multivariate random-effects logistic regression, with hospital as the cluster variable.ResultsA total of 17 938 patients (10 007 men [55.8%]; mean [SD] age, 70.6 [12.2] years) underwent surgery for colorectal cancer: 7796 (43.5%) during the pandemic period and 10 142 (56.5%) during the prepandemic period. Logistic regression indicated that the pandemic period was significantly associated with an increased rate of advanced-stage colorectal cancer (odds ratio [OR], 1.07; 95% CI, 1.01-1.13; P = .03), aggressive biology (OR, 1.32; 95% CI, 1.15-1.53; P < .001), and stenotic lesions (OR, 1.15; 95% CI, 1.01-1.31; P = .03).Conclusions and RelevanceThis cohort study suggests a significant association between the SARS-CoV-2 pandemic and the risk of a more advanced oncologic stage at diagnosis among patients undergoing surgery for colorectal cancer and might indicate a potential reduction of survival for these patients.

Publisher

American Medical Association (AMA)

Subject

General Medicine

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